Abstract

Salicylic acid (SA) is an endogenous growth regulator of phenolic nature and also a signaling molecule, which participates in the regulation of physiological processes in plants such as growth, photosynthesis, and other metabolic processes. Several studies support a major role of SA in modulating the plant response to various abiotic stresses. It is a well-founded fact that SA potentially generates a wide array of metabolic responses in plants and also affects plant-water relations. This molecule also found to be very active in mitigating oxidative stress under adverse environmental conditions. Since abiotic stress remained the greatest constraints for crop production worldwide, finding effective approaches is an important task for plant biologists. Hence, understanding the physiological role of SA would help in developing abiotic stress tolerance in plants. In this chapter, we will shed light on the recent progress on the regulatory role of SA in mitigating abiotic stress.

1. Introduction

Abiotic stresses are a potential threat to agricultural productivity all over the world. Anthropogenic activities provoked the degradation of the agricultural system. Drought, excess soil salinity, extreme high, and low temperatures, metals/metalloids, ozone, UV-B radiation, nutrient (deficiency and excess) are the abiotic stresses which have increased many more times than previous due to anthropogenic activities [1, 2]. It has been projected that abiotic stresses may adversely affect 70% yield of staple food crops and decrease overall crop production by more than 50% [3, 4]. Thus, to improve plant performance and to reduce the loss of productivity caused by abiotic stress is vital. This can be implemented through various approaches and one of those is the application of exogenous phytoprotectant molecule.

2. Biosynthesis and metabolism of SA

Salicylic acid biosynthesis can occur through two distinct pathways viz. isochorismate (IC) pathway and phenylalanine ammonia-lyase (PAL) pathway (Figure 1). Both IC and PAL pathways are started with chorismic acid. Chorismic acid is the end product derived from the shikimic acid pathway in plastid [22–24]. Chorismic acid is converted to IC by isochorismate synthase (ICS) as reported in several plant species [25–27]. Isochorismate pyruvate lyase (IPL) supposed to catalyze the conversion of IC to SA (but the mechanism is not clear) [28].

In PAL pathway, deamination of phenylalanine is accomplished by the activity of PAL which generates trans-cinnamic acid. Trans-cinnamic acid is converted to intermediate product ortho-coumaric acid or producing the benzoic acid which later on produces SA [29–31].

After biosynthesis, SA can be modified into different other forms. Glucosylation of SA generates salicyloyl glucose ester (SGE) and salicylic acid 2-O-β-glucoside (SAG) where the activity of UDP-glucosyltrasferase is involved [32]. The SAG can be stored in the vacuole. Methylation of SA is occurred by SAM-dependent carboxyl methyltransferase to produce methyl salicylate (MeSA) [33]. After production, MeSA is transported to different parts of the plant. Through amino acid conjugation with SA, salicyloyl-l-aspartic acid (SA-Asp) generates (GH3-like phytohormone amino acid synthetase is proposed enzyme catalyze this reaction). SA-Asp can undergo through further catabolism [34]. The conversion of SA to SA-2-sulfonate is proposed to catalyze by sulfotransferase and this process is termed as sulfonation [35]. Hydroxylation of SA is responsible for the production of 2,5-dihydroxybenzoate (Gentisic acid) but the enzyme is unknown [36, 37].

Modifications of SA often render it inactive but these modifications are also related to accumulation, function, and/or mobility. Glucosylation inactivates SA and allows vacuolar storage. Methylation inactivates SA and increases its membrane permeability, volatility which is vital for long-distance transport of this defense signal. Amino acid conjugation of SA is involved in SA catabolism [37].

3. Salicylic acid and abiotic stress tolerance

As a phytohormone, the role of SA in regulating plant growth and development is well known. The role of SA in mitigating abiotic stress has widely been studied since last few decades (Tables 1–4). A large volume of research reports indicate that both endogenous SA synthesis and exogenous application enhance plants tolerance to salinity [38–42], drought [43–45], extreme temperature [46–49], toxic metal and metalloids [50–53], and others [54–58]. Exogenous SA showed enhanced plant growth, photosynthesis, and decreased ROS production under various abiotic stresses (Tables 1–4 and Figure 2).

Plant species

Salinity level

Effect of salinity

SA application

Protective effects

Reference

V. radiata L. cv. Pusa Vishal

100 mM NaCl, 20 d

TBARS and H2O2 contents increased 2.5 and 4-times respectively, compared to control

Na+ and Cl− accumulation increased more than 3-times compared to control

Activity of GR, contents of GSH and GSSG increased compared to control

Table 4.

Summary of the protective roles of SA in mitigating toxic metal/metalloid–induced damages in different crop plants.

Figure 2.

Some possible ways of SA-induced oxidative stress tolerance to plants.

3.1. Salinity

Among the prevailing catastrophic abiotic stresses, salinity or salt stress can be considered as the most devastating one. It shows enormous negative effects, both direct and indirect, on morphological, physiological and biochemical attributes of plants. When plants are exposed to salt, they not only face osmotic and ionic stresses, but also water stress and other subsequent stresses may emerge. These ultimately reduce the quality and quantity of the desired yield. However, good news is there are certain species that show some tolerance mechanisms and also some protectants that can help plants to develop tolerance against the salt stress. In the recent era where global warming and rising of sea level are the most alarming issues, these can be promising facts to be considered for further research. There are a number of studies that prove the protective roles of SA against salt stress in many plant species (Table 1).

Salicylic acid has been proved to have effective roles on enhancing the germination percentage, shoot and root length, fresh weight (FW) and dry weight (DW) of both shoot and root of plants, uptake of beneficial ions, and also some antioxidant enzyme activities. It also has been proved to reduce the toxic ions uptake and accumulation in plants, membrane damage and transpiration rate, etc. Photosynthesis, growth, and yield were improved and oxidative damages were ameliorated with the application of effective concentrations of SA in different plant species. To demonstrate the role of SA in alleviating the salt stress-induced damage, an experiment was conducted by Arfan et al. [59] with two Triticum aestivum varieties, of which one is salt-tolerant (S-24) and another one is salt-sensitive (MH-97). They applied different levels of SA starting from 0.25 to 1.00 mM and created salt stress with 150 mM NaCl in the growing media. Both SA and NaCl were exposed to plants from the very beginning and data were taken at 30 days after sowing (DAS). Their results showed that at lower concentration (0.25 mM) SA could reduce the negative effects of salt on the shoot and root FW and DW in tolerant variety, but this was true at higher concentration (0.75 mM) for the sensitive one. However, yield attributes such as grain yield and 100-grain weight were increased in both the varieties at lower concentrations (0.25 and 0.50 mM) SA under salt stress. Similarly, application of SA also increased the water use efficiency (WUE) of those varieties. Similarly, Nazar et al. [12] also chose two such varieties of Vigna radiata cvs. Pusa Vishal (salt-tolerant) and T44 (salt-sensitive). They also used different concentrations of SA (0.1, 0.5, and 1.0 mM) against 50 mM NaCl stress and 0.5 mM was concluded as the most suitable concentration for both varieties irrespective of their tolerance ability. At this concentration, V. radiata seedlings could reduce the accumulation of toxic Na+ and Cl− ions, and increase S and N uptake and nitrate reductase activity. Salicylic acid application also enhanced the water and osmotic potential which was higher in the tolerant one. Stomatal conductance (gs), intercellular CO2 concentration (Ci), and chlorophyll (chl) fluorescence were increased along with leaf ATP-sulfurylase activity. However, mainly the reduction of electrolyte leakage (EL), malondialdehyde (MDA), H2O2, oxidized glutathione (GSSG) contents, superoxide dismutase (SOD) activity and enhancement of reduced glutathione (GSH) content, and ascorbate peroxidase (APX) and glutathione reductase (GR) activities prove the role of SA in reducing salt-stress damages. Similar results were observed with V. radiata seedlings. These seedlings were exposed to 100 mM NaCl at 10 DAS and then was spraying SA (0.5 mM) at 15 DAS. At 30 DAS some parameters were monitored related to gas exchange e.g., net photosynthesis (Pn), gs, and Ci; and also carboxylation efficiency, WUE, and plant dry mass [17]. Application of SA increased Pn, gs, and Ci by 17.9, 19.2, and 23.5%, respectively, under salt stress condition. It also enhanced carboxylation efficiency and WUE compared to salt-stressed plants. Plant dry mass was increased by 25.2% under salt condition compared to control plants. Meanwhile, Zea mays was tested with different levels of SA under salt stress, and positive roles of SA was demonstrated in ameliorating the membrane damage by reducing MDA content [60]. It can also decrease the accumulation of Na+ and Cl− ions and increase uptake of N and P and thus render tolerance to plants against salt stress. Another experiment was conducted with Lens esculenta, which included only four with Lens esculenta, which included only four treatments: nonsaline control (I), 0.5 mM SA (II), 100 mM NaCl (III), and the combination of 100 mM NaCl + 0.5 mM SA (IV). The results showed that growth parameters: germination (%), shoot and root length, FW and DW were improved in treatment (IV) compared to treatment (III). In addition, SA increased the free Pro and GB content in shoot and also the activities of pyrroline-5-carboxylate reductase (P-5-CR) and γ-glutamyl kinase which are the enzymes related to Pro anabolism. But, in contrast, it reduced the activity of Pro oxidase [61]. In the case of pretreatment with SA, it also showed some positive results. Solanum lycopersicum seeds pretreated with 10 μM SA improved the chl content and reduced MDA content under salt stress (100 mM NaCl) [38]. Higher accumulation of abscisic acid (ABA) in shoot and enhancement of water potential of SA-treated seedlings compared to the seedlings exposed to salt alone were also observed [38]. These results were supported by Horváth et al. [62] in the same plants with the equal concentrations of SA. Similarly, when pretreatment with SA (0.5 and 1.0 mM) was done, Gerbera jamesonii seedlings also showed positive results in salt stress (100 mM). Salicylic acid application reduced the EL, MDA and Pro contents and increased the activities of SOD, catalase (CAT), peroxidase (POD), and APX compared to salt stressed seedlings [39]. But, these effects were more acceptable in case of lower (0.5 mM) concentration of SA. Recently, Nazar et al. [41] again used SA (0.5 mM) to demonstrate the preventive role of it in Brassica juncea seedlings exposed to 100 mM of NaCl stress for 30 consecutive days. Application of SA reduced thiobarbituric acid reactive substances (TBARS) and H2O2 contents, also dehydroascorbate (DHA) and GSSG contents. It was found to increase the activities of dehydroascorbate reductase (DHAR), APX, and GR to a remarkable content. And most importantly, it reduced the toxic Na+ and Cl− uptake to almost half of the salt-stressed plants [41].

From the above-mentioned studies, the role of SA in alleviating salt stress can be considered as clear and concise. But, there are also some points to be considered as higher concentrations of SA may itself cause damage to plants [12, 59] and very lower concentrations may have a minimum effect [42, 62] against salt stress. So, the concentration of SA, application method and time, duration of salt stress and plant age are some of the important points to be considered while using SA against salt stress.

3.2. Drought

Drought stress is one of the most devastating abiotic stresses adversely affecting growth and developmental processes of the plant. Drought stress affects the physiological processes, brings biochemical changes, leads to the formation of secondary metabolites, significantly accumulates endogenous reactive oxygen species (ROS) and increases toxins (such as methylglyoxal). Drought stress hampering the reproductive development drastically reduces yield or productivity of plants [67].

Several studies demonstrated and proved the pivotal roles of SA in alleviating drought damage and improving drought stress tolerance in plants (Table 2). Salicylic acid pretreatment (0.5 mM) alleviated substantial water loss and its damaging effects on wheat seedlings that enhanced drought tolerance [43]. Pretreatment with SA upregulated 37 protein spots under drought stress which has been investigated through proteomics. Glutathione S-transferases, APX, and 2-cysteine peroxiredoxin were enhanced under drought stress. Enhancement of antioxidant defense system worked against the oxidative damage [43]. Proteins involved in ATP synthesis are also upregulated by SA under drought stress. Salicylic acid supplementation with drought also upregulated 21 protein spots, including RuBisCo and related enzymes [43]. In their other experiment, influential role of SA was also demonstrated on AsA-GSH cycle [68]. Exogenous SA supplementation enhanced the transcription of GST1, GST2, GR, and MDHAR genes during almost the entire drought period. The increase of DHAR was noticed at 12 h, GPX1 at 48 h, phospholipid hydroperoxide glutathione peroxidase (GPX2) at 12 and 24 h, and glutathione synthetase (GSHS) at 12, 24, and 48 h of drought stress. Upregulation of transcription level of AsA-GSH cycle enzymes contributed to drought tolerance [68]. SA-accumulating (siz1 and cpr5) genes were highly expressed in guard cells of drought which modulated movement of stomatal aperture in Arabidopsis plants. The generation of ROS was also modulated in this plant [69]. In tomato (Lycopersicon esculentum), SA treatment with drought has been demonstrated to protect the activity of nitrate reductase which helps to maintain the protein and nitrogen contents of the leaves, compared to the drought affected plant without SA addition. Photosynthetic parameters, membrane stability, water potential and activity of carbonic anhydrase were maintained by SA which also contributed to drought stress tolerance [70]. In sunflower, water stress-induced decrease in the yield and oil content. Salicylic acid (0.724 mM) application increased the Pro content, head diameter, number of achene, 1000-achene weight, achene yield, and oil yield of sunflower, compared to drought treatment alone [71]. The addition of acetyl SA in (0.1–1.0 mM) also improved drought tolerance of muskmelon seedlings [72]. Two wheat varieties viz. Wafaq-2001 and Punjab-96 were subjected to drought stress. Drought stress significantly decreased membrane stability index (MSI) and yield. Salicylic acid supplementation caused 37% increase in soluble sugars in Wafaq-2001 cultivar which was higher, compared to Punjab-96 cultivar. Salicylic acid also increased protein content and MSI in both cultivars with a higher increase in Wafaq-2001. The overall drought tolerance was higher in Wafaq-2001 after SA application which is evident from higher yield [73]. Exogenous addition of SA increased the activity of antioxidant enzymes which helped to alleviate the drought stress damage in Ctenanthe setosa [74]. Mustard (B. juncea L. cv. BARI Sharisha 11) seedlings were subjected to two different levels of drought with 10 and 20% polyethylene glycol (PEG) for 48 h. Leaf relative water content (RWC), chl b and chl (a + b) decreased but Pro content increased. Disrupting the antioxidant defense system, drought stress increased oxidative damage which was indicated by high MDA and H2O2 levels. Supplementation of SA in drought-stressed seedlings increased the leaf RWC and chl content, increased the AsA and GSH, decreased the GSSG content, and maintained a higher ratio of GSH/GSSG. Salicylic acid increased the activities of monodehydroascorbate reductase (MDHAR), DHAR, GR, glutathione peroxidase (GPX), CAT, glyoxalase I (Gly I), and glyoxalase II (Gly II) in drought affected seedlings as compared to the drought-stressed plants without SA supplementation, with a concomitant decrease in H2O2 and lipid peroxidation level [44]. Methyl-SA (at 0.1 mM) spray promoted drought-induced leaf senescence in Salvia officinalis [75]. Drought stress adversely affected growth performance of winter wheat, Cheyenne. Application of SA analogue 4-hydroxybenzoic acid (4-HBA) increased drought tolerance of winter wheat Cheyenne [16]. Foliar application of SA (10 μM) protects lemongrass (Cymbopogon flexuosus Steud. Wats.) varieties (Neema and Krishna) from drought stress by improving growth parameters, modulating the activities of nitrate reductase, carbonic anhydrase, and EL, Pro content, free amino acid, and in PEP carboxylase activity [76].

3.3. Extreme temperatures

Temperature is one of the vital factors that determine plants establishment, growth, development, and productivity. Due to climate change, global average temperature is fluctuating very rapidly and threatening the survival of living beings. Thus, among the various abiotic stresses, extreme temperature has become the talk of the topic in recent decades because of its devastating and damaging effects on plants [84]. Extreme temperature includes both high temperature (HT) and low temperature (LT) that can injure plants. The high temperature is the increasing of temperature beyond the critical threshold level that can deplete plant growth and metabolism depending on the sufficient time period [85]. Heat stress often becomes worse because of its combination with other stresses including drought [86]. High temperature severely alters the plant physiological processes including germination, photosynthesis, respiration, transpiration, partitioning of dry matter, etc. [87]. In addition, HT results in enzyme inactivation, protein denaturation, disruption of proteins and membranes which ultimately affects plant growth [88, 89]. Low-temperature consists of both freezing (<0°C) and chilling (0–15°C) temperatures. In chilling stress plant faces injury without formation of ice whereas, in freezing stress, the formation of ice occurs in plant tissues. Chilling and freezing stresses are together called cold stress or LT stress. Low-temperature stress shows various damaging symptoms in plants including faster senescence and decay [90, 91], interference with germination, cell membrane disruption, photosynthesis, water and nutrients uptake, reproductive development as well as growth and yield [92]. Either HT or LT conditions, at molecular level, leads to the overproduction of ROS which ultimately gives rise to the oxidative stress [84, 93]. Nowadays, to develop temperature-stress tolerance, the use of exogenous SA is one of the common approaches. Salicylic acid being the endogenous growth regulator or phytohormone acts as an important signaling molecule and develops abiotic stress tolerance in plants [94]. Recent advances on SA-mediated temperature stress tolerance have been listed in Table 3.

3.4. Toxic metal/metalloids

In the industrial era, the most important and potential threat for crop production is the abiotic stress. Among them, toxic metal stress is one of the major concerns. Growing population and fast industrialization coincide together, results in the generation and dissemination of huge amount of toxic metals in the environment [110]. Toxic metal consists of a set of harmful elements having no biological role in organisms such as Cd, Pb, Hg, St, Al, etc. Although toxic metals and heavy metals (HMs) are often thought to be synonymous, some lighter metals such as Al may also cause toxicity. Toxic and HMs are differed in the case of their biological role. Some HMs having a biological role in plants also considered toxic when they are used in high concentrations, viz. Ni, Cu, Zn, etc. On the other hand, metalloid includes those elements that show behavior both like metals and nonmetals including B, Si, Ge, St, As, Sb, etc. The underlying parent material and atmosphere are the two main sources of toxic metals. Metals are uptaken and accumulated easily by plants and causes toxicity within the plant tissue. They directly interact with the proteins, enzymes, and causes phytotoxicity. The inhibition of growth rate is the most certain consequences of metal toxicity [111]. Leaf rolling, chlorosis, necrosis, stunted growth, stomatal dysfunctioning, cation efflux, reduced water potential, alterations in the membrane, photosynthesis, metabolism, and various key enzymes are some other toxic metal effects in plants [111, 112]. Toxic metals also manipulate the nutrient homeostasis, water uptake, transport, transpiration, respiration, and ultimately may lead to plant death [113, 114]. Metal toxicity at the cellular level results in the overproduction of ROS [110]. To mitigate metal induced stresses in plants, plant biologists are trying to develop new strategies. Salicylic acid is a very important molecule that induces defense responses against various toxic metal/metalloids stresses (Table 4).

Several research findings demonstrated that exogenously applied SA improved the growth and photosynthetic traits in different plants by reducing the damaging effects of toxic metals. O. sativa exposed to As (25 and 50 μM) [50], A. thaliana exposed to As (100 μM) [115], T. aestivum exposed to Cd (500 and 1000 μM) [121], and Z. mays exposed to Cr (500 ppm) [52] grown well under SA supplementation. In a recent study, SA pretreatment reduced the oxidative stress in T. aestivum after Cd (0.01, 0.1, and 1 mM) exposure. Cd stress increased the lipid peroxidation and EL percentage. But the exogenous application of SA significantly declined the MDA content and EL percentage [53]. Salicylic acid also evidenced to alleviate the oxidative stress induced by metal toxicity in several other plant species by decreasing the toxic effects of overproduced ROS and lipid peroxidation. In O. sativa, enhanced MDA and H2O2 contents induced by As (25 and 50 μM) were reduced by the exogenous SA pretreatment [50]. Similarly, adverse oxidative stress was also demonstrated in Lolium perenne as induced by Cd (100 μM). Results showed that increased accumulation of O2•−, H2O2, and higher MDA were decreased by SA application. Some other research findings also supported that the SA mitigates metal-induced oxidative damage in Pisum sativum [136], Brassica oleracea var. botrytis [135], Medicago sativa [134], etc. It was reported that treatment with SA alleviated the Cd (15 μM) induced root growth inhibition and improved the antioxidant activities thus reduced the Cd-induced oxidative stress in Hordeum vulgare [51]. Salicylic acid supplementation in As (100 μM) stressed A. thaliana showed improved performance in terms of antioxidant enzymes (APX, CAT, SOD) activities and enhanced tolerance to metal stress. In other experiment it was demonstrated that when SA was exogenously applied against Cd (0.25, or 0.50 mM) stress, increased amelioration of metal stress was observed with increasing activities of defense responsive genes and upregulating the antioxidant (SOD, CAT, APX, and GR) enzymes [117]. Decreased root growth, RWC, and increased oxidative stress were decreased by seed priming with SA [118]. Under Cd (50 and 100 mM) stress, plant growth, chl, total lipid contents, and nutrient absorption became decreased which were further increased by soaking seeds with SA. Increased stress tolerance with reduction of oxidative damage was also evident [119]. Increased ROS production, TBARS content, and EL with increased SOD, CAT, and APX activities were found after Cd (50 and 100 μM) exposure. Seed priming with SA significantly decreased the oxidative damage and increased the antioxidant enzymes activities. Agami and Mohamed [121] reported that SA efficiently alleviated the adverse Cd (500 and 1000 μM) stress by restoring the growth parameters and increasing the antioxidant defense system. Exogenous SA developed Cr (mg L−1) stress tolerance by improving growth, photosynthetic pigments and oxidative stress reduction by upregulating antioxidant defense system [52]. Inhibited antioxidant enzymes (APX, CAT, POX, and SOD), soluble sugars and chl contents were showed when T. aestivum exposed to Pb (10, 50, 100, 200 mg L−1). Alleviated inhibitory effects were found after SA supplementation as cotreatment [126]. In Zygophyllum fabago, increased Pb accumulation after Pb (0.75 mM) exposure was reduced by SA pretreatment. Upregulated antioxidants and downregulated oxidative damage together induced stress tolerance [125]. Salicylic acid treatment against Cd (5, 10 or 50 mM) stress increased tolerance in P. pratensis by controlling uncontrolled absorption of Cd and maintaining nutrients (K, Ca, Fe, Mg) homeostasis [127]. Effects of B was investigated (25 and 50 mg kg−1) toxity in Daucus carota and S. oleracea. In both plants, the growth, physiology, and antioxidant enzymes activity were affected by B toxicity. But exogenous SA application showed some protective effects in the alleviation of the metal toxicity [128, 129]. A similar finding was also demonstrated by Shi and Zhu [131] in Crocus sativus plant. Exposure to a toxic level of Mn (600 μM) with SA in C. sativus plant, maintained nutrient (Ca, Mg, Zn) homeostasis, reduced metal stress, and improved tolerance. Recent findings in B. juncea against Mn (3, 6, or 9 mM) toxicity revealed that SA is an important regulator of photosynthetic enzymes including carbonic anhydrase (CA). It together with the upregulated defense system and reduced oxidative damage-regulated the photosynthesis in a concentration-dependent manner [130]. Besides upregulation of antioxidant enzymes, SA involved in the activation of CaM-like protein genes and cytosolic Ca2+ in Al (30 μM) stressed Glycine max. It has been showed that increased metal stress tolerance resulted from exogenous SA treatment [132]. Effect of exogenous SA was investigated upon Pb (50 μM) stressed Vallisneria natans. Decreased chl, carotenoid, NADPH oxidase, nonprotein thiols, AsA but increased CAT, DHAR, and POD activities were observed. Pretreatment with SA increased the activities of NADH oxidase, AsA, and GSH in Hg (10 μM) stressed M. sativa and thus developed better tolerance to stress [133]. Recent evidences suggested that SA develops stress tolerance by involving in the regulation of photosynthetic pigments, activities of CA, NR, and anticancer alkaloids (vincristine and vinblastine) upon Ni (50, 100, and 150 mg kg−1) exposure in Catharanth roseus [122]. Toxic level of Ni (0.5 mM) impacts on Brasicca napus also suggested that application of SA decreased the leaves’ toxicity symptoms (chlorosis, necrosis, etc.) and improved growth and survival [123]. Recently a combined effect of metals (Co, Ni, Cd, Cr, and Pb) (0.25 M) on B. oleracea var. botrytis has been investigated. It has been found that SA alleviated all the toxic effects of metals except for Cr. In the case of Cr, SA accelerated the toxic effects and the plant died [135]. Improved CO2 fixation, RuBPC activity, and chl content were found in Cd (0.5, 1, 2, and 5 μM) stressed P. sativum when supplied with exogenous SA.

3.5. Ozone and ultraviolet radiation

Due to the gradual increase in atmospheric ozone (O3) concentration, it has become a major threat for plant species mainly because of its pollutant and photochemical oxidant affects [139]. Significant crop losses due to O3 damage is predicted to be increased by 25% in background O3 concentration over the next 30–50 years [140]. High concentrations of ozone induce oxidative stress, which activates programmed cell death and significantly inhibits plant growth, causing plant death and loss of quality [141]. It is the most noteworthy atmospheric pollutant in terms of phytotoxicity. It is to be noted that in the concentration of O3 has been decreased by 5% in the past 50 years due to the release of anthropogenic pollutants and, a larger proportion of the UV radiation (especially (UV-B) spectrum reaches the Earth’s surface [142]. Although sunlight plays an integral role in harvesting light energy through photosynthesis, high light, especially ultraviolet (UV) radiation, resulted in stress to plants, which include damage to DNA, proteins, and other cellular components [143]. This episode is unavoidable as 7% of the electromagnetic radiation emitted from the sun is in the UV range (200–400 nm). UV radiation also leads to oxidative stress by photooxidation and excess generation of ROS [84]. To cope up the adverse effects of both O3 and UV radiation needs some adaptive mechanisms. In few plant species, SA was found to take part in enhancing the tolerance to O3 and UV radiation mainly by enhancing antioxidant defense and improving plant growth.

In A. thaliana, UV-C light stress activated the transition to flowering through SA. SA could regulate the time of flowering by inducing photoperiod and autonomous pathways which are evident by late flowering in SA-deficient plants. While investigating the genes responsible for flowering induction viz. constans (CO), flowering locus T (FT), suppressor of overexpression of constans 1 (SOC1), and flowering locus C (FLC) it was observed that the expression of CO, FT, and SOC1 transcripts decreased to around 50% in long day-grown SA-deficient plants when compared to contron plants [54]. In short day plants, only the levels of FT transcripts were reduced compared to CO. Thus, it indicated that SA might play important role in flowering under UV radiation [54]. The effect of UV was investigated (UV-A: 320–390 nm, UV-B: 312 nm, and UV-C: 254 nm radiation with a density of 6.1, 5.8, and 5.7 W m−2) on Capsicum annuum plants and found that activities of antioxidant enzymes were enhanced in leaves in response to UV-B and UV-C radiation. Moreover, SA treatment showed further enhancement in the activities of POD, APX, CAT, and GR while some other enzymes were modulated [55]. In another report, a clear decline was reported in photosynthetic pigments (chl a, chl b, and carotenoid) under UV-A, UV-B, and UV-C, while a foliar spray of SA recovered this decline. The level of anthocyanins, flavonoids, and rutin in SA-treated plants was also higher than in a UV-exposed plant grown without SA [56]. V. radiata, exposed to UV-B radiation (ambient + 4–8 kJ m−2) showed declined growth, photosynthetic pigments and photosynthesis (Fv/Fm and qP except NPQ) which were accompanied by significant decrease in SA level [57]. UV radiation also causes overproduction of ROS and concomitantly damaging effects on lipids, proteins, and membrane stability. However, SA pretreatment significantly alleviated the adverse effects. They also revealed that UV-B altered SA biosynthesis and SA-pretreatment might act as a signal that reduces oxidative stress by triggering upregulation of antioxidant defense and subsequent improvement of growth and photosynthesis [57]. In Satureja hortensis, both UV-B and UV-C exhibited decreased plant growth (plant height, root length, shoot DW, and leaf area), node number, internode distance and chl content, while stem diameter, leaf thickness, flavonoid content, phenolic content, and antioxidant activity were increased [58]. The increase in secondary metabolite such as flavonoid content, phenolics might be able to protect cells against free radicals but this level was not well enough under severe stress. On the other hand, plants treated with 1 mM SA exhibited higher growth and improved physiology compared to nontreated one and subsequently showed better appearance under UV radiation [58].

4. Salicylic acid and ROS detoxification

Salicylic acid is the most studied phytohormone regarding its role in oxidative stress. Due to its multifarious actions, it has been found very effective in detoxifying ROS in plant cells (Figure 2). According to Janda and Ruelland [144], SA-induced tolerance to abiotic stresses such as chilling, heat, heavy metals, osmotic stress, and salinity is involved in activation of the stress-induced antioxidant system. It has been demonstrated that SA could significantly improve both photosynthesis parameters and antioxidant defense system in conferring salt stress tolerance in V. radiata [17]. In O. sativa, exogenous SA significantly reduced the oxidative burst by reducing H2O2 and O2•− contents under herbicide exposure which was mainly due to the SA-mediated upregulation of antioxidant defense enzymes (SOD, POD, CAT, APX, GR, and GST) and efficient GSH pool. The positive role of SA is mostly dependent on their dose and application methods [145]. Other study also proved that SA-mediated antioxidative defense system was dependent on the concentration used and the method of application [146]. In T. aestivum, 0.25 mM SA resulted in marked increase in the antioxidant enzyme activities (SOD, CAT, POD, GPX, APX, and GR), while the treatment with 2.5 mM SA resulted in a decrease in the activities under water stress [146]. A lower dose of SA also maintains higher AsA pool which in turns significantly scavenged the ROS. This ROS detoxification induced by SA also associated with improved photosystem II (PSII) efficiency. Belkadhi et al. [147] showed that Linum usitatissimum plants showed a lower amount of lipid and protein oxidation and membrane oxidation under Cd stress when pretreated with SA. This protection was availed by the enhanced activities of SOD, GPX, and APX as well as the 2,2′-diphenyl-1-picrylhydrazyl (DPPH) scavenging activity and ferric-reducing antioxidant power (FRAP). Increases in MDHAR, DHAR, GR, GPX, and CAT activities 53, 64, 49, 82, and 65% were noticed in PEG-treated B. juncea seedlings when sprayed with 50 μM SA [44]. SA-induced upregulation of antioxidant enzymes caused 32 and 26% decrease in MDA and H2O2 content compared to drought (20% PEG, 48 h) alone. One of our research results showed that exogenous SA enhanced the activities of antioxidant enzymes and nonenzymatic antioxidants under salt stress (200 mM NaCl, 48 h). Compared to salt stress alone, NaCl + SA resulted in 41, 107, 25, 37, 44, and 59% increases in MDHAR, DHAR, GR, GST, GPX, and CAT activities [40]. Salicylic acid supplementation also increased AsA and GSH content by 48 and 39%, respectively and enhanced GSH/GSSG ratio by 47% compared to salt stress alone. As a result, MDA and H2O2 contents decreased by 39 and 31% [40]. In Nitraria tangutorum SA mitigated salt-induced oxidative stress (evidenced by a marked reduction in MDA and H2O2 content) by upregulating the activities of SOD, POD, and CAT. The content of MDA in the 1.5 mM SA treated seedlings under 100–400 mM NaCl treatments declined to 2.27–3.59 fold of the control which was a clear sign of the reduction of oxidative stress [148]. However, some of the enzymes like APX activity was inhibited at higher concentrations (1.0 and 1.5 mM) of SAMDA content was measured with 1.5 mM SA applied, and the contents of MDA in the leaves of SA-treated seedlings under 100–400 mM NaCl treatments declined to only 2.27–3.59 fold of the control.

5. Interaction of SA with other signaling molecules

Salicylic acid not only exerts its positive effect independently but also interacts with other signaling molecules, phytohormones, and other phytoprotectants. These interactions show different signaling events and ultimate protection to plants from stress-induced damages (Figure 3). In grapevines, Wang and Li [102] showed improved Ca2+ homeostasis and associated antioxidant defenses under heat and cold stress-regulated by SA. When plants were treated with exogenous SA, they showed enhanced PM-Ca2+ATPases and V-Ca2+ ATPases activities. Moreover, Ca2+ precipitates were shown on the inner side of the plasma membrane, and less were in intercellular spaces and the vacuole. However, in SA treated plants Ca2+ precipitates were in vacuoles, and few were on the inner side of the plasma membrane. Ca2+ precipitates in chloroplasts were bigger even after heat or cold stress. Importantly, SA treatment caused enhancement of the activities of APX, GR, and MDHAR, which efficiently reduced the lipid peroxidation and relative EL (REL), which concluded that exogenous SA could mitigate oxidative stress by maintaining Ca2+ homeostasis under extreme temperature stress [102]. In O. sativa, Wang et al. [145] reported that SA treatment downregulated ABA genes more in cultivar XS 134, which correlated with the enhanced tolerance to quinclorac-induced oxidative stress. Application of SA had obvious effects on all of the ABA-related genes and inhibited the expression of OsABA8ox1, OsABA8ox2, OsABA8ox3, OsNCED1, OsNCED2, and OsNCED3 as compared to quinclorac stress alone. Since overproduction of ABA and ROS is highly associated this downregulation protected the plants from herbicide-induced damages. Wang et al. [145] also reported SA-induced inhibition of ABA synthesizing enzymes. Leslie and Romani [149] reported that SA inhibited ethylene formation which triggered biosynthesis of ABA under stress conditions [150]. In the adventitious roots of Panax ginseng, SA-induced enhancement of the activities of NADPH oxidase, SOD, CAT, POD, and APX was evident while no significant effect on AsA and GSH content were observed [151]. These effects were mostly NO-dependent and it was also observed that SA-induced the generation of NO. They revealed that at lower concentration (100 μM) SA was highly effective in inducing the accumulation of NO, O2•− and it took part in stress signaling. Interactive effects of SA and NO were studied in mitigating osmotic stress (−0.4 MPa) in T. aestivum. It was observed that osmotic stress induced chl degradation and membrane instability, and H2O2 generation and lipid peroxidation were effectively reduced by exogenous application of SA or SNP, which was associated with the enhancement of antioxidant defense. However, pretreatment of plants with methylene blue (MB; as a guanylate cyclase inhibitor) reversed or reduced the protective effects of SA and SNP suggesting that the protective effects were likely attributed to NO signaling. They also concluded that NO may act as downstream of SA signaling in the reduction of induced oxidative damage [152]. SA-mediated H2O2 signaling and subsequent Cd stress tolerance was revealed in L. usitatissimum [147]. Seedlings pretreated with 250 or 1000 μM SA resulted in enhanced production of H2O2 because of inhibited CAT activity. Although the control plants with SA pretreatment showed significant (1.2 fold) increase in H2O2, this level is remarkably lower when compared with Cd alone and Cd+SA. These results indicated that SA could regulate the Cd-induced oxidative stress because Cd-treated seedlings primed with SA exhibited a higher level of total antioxidant capacities and increased activities of H2O2-detoxifying enzymes [147]. Exogenous SA application was found to activate GSH synthesis in B. juncea and B. napus and showed enhanced protection against drought- and salt-induced oxidative damages [44, 40].

Figure 3.

Interaction of SA with other signaling molecules to elicit defense responses in plants.

6. Conclusions and perspectives

Salicylic acid plays an important role in the regulation of growth and physiology in relation to the abiotic stress responses of plants. The SA was found to be effective in the different form of application foliar spray/incorporation with growing media depending upon plant species. The low concentration of SA showed advantageous effects in abiotic stress tolerance of plants. In contrast, the high concentration of SA showed toxic effects. Thus, both the concentration and application method of SA are critical to obtaining its best effect on different plant species. In the biosynthesis pathway of SA, there are unknown steps and enzymes which should be discovered. The catabolism and the further fate of transformed product of SA are not known clearly. How SA interacts and being regulated by the cross-talk in harmony with other phytohormones and plant growth regulators working (auxins, cytokinins, gibberellins, ethylene, jasmonates, brassinosteroids, etc.) and other signaling molecules (NO, H2O2) were not studied extensively. SA-mediated defense networks and insights into the cross-talk of SA with other defense-signaling pathways should be revealed. An integrated approach combining the knowledge of genetics, molecular biology, biochemistry, genomics, and bioinformatics techniques is a useful tool to study the functioning of SA in plants. Clear understanding of the biosynthesis and catabolic pathway and other unanswered question are vital to exploit SA as a potent phytoprotectant molecule to improve abiotic stress tolerances.

Acknowledgements

We are highly thankful to Mazhar Ul Alam, Laboratory of Plant Stress Responses, Faculty of Agriculture, Kagawa University, Japan, for his critical reading and formatting of the manuscript draft. The first author acknowledges Japan Society for the Promotion of Science (JSPS) for funding in his research. We are also highly thankful to Mr. Md. Mosfeq-Ul-Hasan, Zhejiang University, Hangzhou, China, for providing us several supporting articles. As page limitation precluded us from citing a large number of studies, we apologize to those whose original publications are therefore not directly referenced in this chapter.

Author contributions

M.H. performed literature reviews and drafted the manuscript; K.N., T.I.A. and T.F.B., M.I. and M.H. contributed the review for literature research; M.F. and H.O. reviewed the manuscript and approved the final draft.